Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction

Abstract

The spatial unity of self and body is challenged by various philosophical considerations and several phenomena, perhaps most notoriously the "out-of-body experience" (OBE) during which one's visual perspective and one's self are experienced to have departed from their habitual position within one's body. Although researchers started examining isolated aspects of the self, the neurocognitive processes of OBEs have not been investigated experimentally to further our understanding of the self. With the use of evoked potential mapping, we show the selective activation of the temporoparietal junction (TPJ) at 330-400 ms after stimulus onset when healthy volunteers imagined themselves in the position and visual perspective that generally are reported by people experiencing spontaneous OBEs. Interference with the TPJ by transcranial magnetic stimulation (TMS) at this time impaired mental transformation of one's own body in healthy volunteers relative to TMS over a control site. No such TMS effect was observed for imagined spatial transformations of external objects, suggesting the selective implication of the TPJ in mental imagery of one's own body. Finally, in an epileptic patient with OBEs originating from the TPJ, we show partial activation of the seizure focus during mental transformations of her body and visual perspective mimicking her OBE perceptions. These results suggest that the TPJ is a crucial structure for the conscious experience of the normal self, mediating spatial unity of self and body, and also suggest that impaired processing at the TPJ may lead to pathological selves such as OBEs.

Figure 1.

Stimuli. Four different stimuli as used in the OBT task and the lateralization task are shown. Correct responses in the OBT task are indicated below each figure.

Figure 2.

Behavioral and evoked potential data during OBT task and lateralization task (healthy subjects). A, Reaction times in the OBT task (blue) and the lateralization task (red). On the left, the RTs (OBT task) are plotted separately for front-facing (light blue) and back-facing figures (dark blue). On the right, the RTs [lateralization task (LAT)] are plotted separately for front-facing (light red) and back-facing figures (dark red). Note the longer RTs for the OBT task. Front-facing figures during the OBT task, but not for the lateralization task, were characterized by longer RTs with respect to back-facing figures. B, Segments of stable map topography in the four experimental conditions under the global field power curve from 0 to 700 ms. Evoked potential segment 6 (segment shown in black) was found from ≈330 to 400 ms and only in the OBT task. C, Duration of evoked potential segment 6 (the respective map is shown in the right top corner of the figure) for the four experimental conditions for all participants. The duration of evoked potential segment 6 parallels the behavioral differences in the four experimental conditions. D, Evoked potential recorded at electrode P5 in the four experimental conditions showing differential coding between OBT (blue) and lateralization tasks (red) as well as between front-facing (light blue) and back-facing (dark blue) figures during the OBT task. The black bar estimates the time of differential coding between both tasks and is in agreement with the occurrence of evoked potential segment 6. E, Generators of evoked potential segment 6 (by inverse solution), which were localized bilaterally at the TPJ and predominated at the right TPJ.

Figure 3.

TMS data during OBT and LT tasks (healthy subjects). A, The different stimuli as used in the TMS experiment are shown. Correct responses are indicated to the right of each figure. The effects of TMS on the OBT task (human figures) and the LT task (letter F) were tested in a 2 × 2 block design (2 tasks × 2 TMS sites). B, Normalized RTs for the investigated TMS pulse delays (100-800 ms after stimulus onset) for OBT (left) and LT (right) tasks. The top figures plot the RTs for back-facing human figures (OBT task) and unturned letters (LT task) when TMS is applied over either TPJ (filled triangles) or IPS (open squares). The bottom figures show RTs for front-facing figures (OBT task) and turned letters (LT task) for the same TMS conditions. TMS neither of the TPJ nor of the IPS had any effect on performance to back-facing/unturned stimuli (top figures). TMS of the TPJ slowed RTs to front-facing figures (OBT task) relative to IPS stimulation when TMS was applied between 350 and 550 ms after stimulus onset (bottom left plot). This was concordant with the evoked potential data (time period is indicated by black bar). TMS over IPS, in contrast, increased RTs to turned letters (LT task) relative to TPJ stimulation at TMS pulse delays of 450-600 ms (bottom right plot). Error bars indicate SEs. C, TMS sites at the TPJ and IPS rendered over each subject's cortical surface plot constructed from the individual MRIs.

Figure 4.

Patient data. A, MRI with the implanted electrodes overlying the lateral convexity of the left hemisphere. The epileptic focus, for which the discharge induced an OBE, is indicated by the eight white electrodes at the TPJ. iEP amplitude (in microvolts) for all implanted electrodes during the OBT task at ∼333 ms (blue depicts positive values and red depicts negative values). B, The most prominent iEPs at this latency were recorded at electrode sites 50, 51, 58, and 59 over the TPJ and partly overlapping with the epileptic focus (A). C, Three iEPs during the OBT task, which were recorded in the basal temporal region (indicated by the arrow in A). Although iEPs at these electrode sites were also prominent, they were recorded at a different latency (∼270 ms). Importantly, as shown in E, the amplitude of these basal temporal iEPs did not differ for front-facing (light blue) and back-facing (dark blue) figures, whereas the amplitude of the iEPs at the TPJ did (D). The electrode site for each figure is given in the bottom right corner of each panel.